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Priority Actions to Improve Provenance Decision-Making

MARTIN F. , PETER A. HARRISON, ARMIN BISCHOFF, PAULA DURRUTY, NICK J. C. GELLIE, EMILY K. GONZALES, KAYRI HAVENS, MARION KARMANN, FRANCIS F. KILKENNY, SIEGFRIED L. KRAUSS, ANDREW J. LOWE, PEDRO MARQUES, PAUL G. NEVILL, PATI L. VITT, AND ANNA BUCHAROVA

Selecting the geographic origin—the provenance—of seed is a key decision in restoration. The last decade has seen a vigorous debate on whether to use local or nonlocal seed. The use of local seed has been the preferred approach because it is expected to maintain local and avoid deleterious population effects (e.g., and outbreeding depression). However, the impacts of fragmentation and on populations have driven the debate on whether the local-is-best standard needs changing. This debate has largely been theoretical in nature, which hampers provenance decision-making. Here, we detail cross-sector priority actions to improve provenance decision-making, including embedding provenance trials into restoration projects; developing dynamic, evidence-based provenance policies; and establishing stronger research–practitioner collaborations to facilitate the adoption of research outcomes. We discuss how to tackle these priority actions in order to help satisfy the restoration sector’s requirement for appropriately provenanced seed.

Keywords: assisted migration, ecological restoration, , restoration genetics

he restoration sector’s demand for seed is Williams et al. 2014, Havens et al. 2015, Prober et al. 2015, Tenormous and is rapidly increasing with the growth Breed et al. 2016b, Christmas et al. 2016b). in the global restoration effort (Verdone and Seidl 2017). Consequently, several alternative provenancing strate- Choosing the geographic origin—the provenance (see the gies have been proposed to supplement local provenances glossary in box 1 for definitions)—of seed used in resto- with nonlocal provenances. These strategies generally fall ration is an early and fundamental decision faced by res- into two categories: those that attempt to increase the adap- toration practitioners (Miller et al. 2017). The traditional tive potential of at a restoration site by increasing practice has been to source seed local to the restoration the genetic diversity of the seed mix (e.g., relaxed local, site—local provenancing—because it is expected to maintain composite, and admixture provenancing) and those that the evolutionary history of plant populations (e.g., local recommend matching provenances with anticipated future adaptation), minimize maladaptation, and limit deleterious environmental conditions of a restoration site (e.g., predic- genetic effects (e.g., outbreeding depression). tive and climate-adjusted provenancing). Although there Global change has sparked a broad and robust debate on are theoretical underpinnings to these alternative strate- whether nonlocal seed should be used in restoration and, if so, gies, experimental field-testing in restoration contexts is under what circumstances (Hamilton 2001, Wilkinson 2001, limited. Broadhurst et al. 2008, Mijnsbrugge et al. 2010, Byrne et al. In this article, we identify several knowledge gaps and 2011, Breed et al. 2013, Williams et al. 2014, Havens et al. practical barriers that need priority action by researchers, 2015, Prober et al. 2015, Breed et al. 2016b, Christmas et al. policymakers, and practitioners to improve provenance 2016b, Bucharova 2017). There are two central tenets to this decision-making from an international perspective. We argument: and climate change. Habitat ­discuss these priority actions in light of the global restora- fragmentation generally increases and reduces tion challenge of restoring degraded terrestrial landscapes effective population sizes of plant populations, which can from grassland to forest , but we acknowledge have an impact on local seed quality by reducing fitness and that the success of a provenancing strategy will be context adaptive potential (Vranckx et al. 2011, Breed et al. 2015). dependent (e.g., landscape heterogeneity and age; plant Because climate is a strong and common agent of selection ­, demography, and evolutionary ­history; and in plants (Davis and Shaw 2001, Petit et al. 2008), it has been management priorities, scale, and resources). By highlight- argued that provenance selection should match values of cli- ing these priority actions, we hope to improve support for matic variables predicted into the future (Breed et al. 2013, restoration, offer guidance for policy development, bridge

BioScience 68: 510–516. © The Author(s) 2018. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights reserved. For Permissions, please e-mail: [email protected]. doi:10.1093/biosci/biy050 Advance Access publication 7 June 2018

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Box 1. Glossary of terms.

Admixture provenancing: Supplementing local provenances with seed collections across a species’ natural distribution. Climate-adjusted provenancing: Supplementing local provenances with targeted nonlocal provenances collected along a climate gradient in line with climate-change projections. Composite provenancing: Supplementing local provenances with seed from multiple nonlocal provenances within gene-flow dis- tances to mimic natural among populations. : The of a genotype for favorable attributes such as fast growth or high-salinity (or other extreme environ- ment) tolerance. Habitat suitability model: A model of the statistical relationship between species occurrences and environment that conceptually represents the predicted spatial abiotic and biotic limits of a species suitable habitat. These models are also referred to as species distri- bution models or models and draw on ecological niche theory. : The increased fitness of the product between two divergent provenances or species compared with parental genotypes. Local adaptation: Superior fitness of a local population over other provenances when grown in its home environment. Local provenance: Seed from either within the restoration site (strict local provenance) or within close geographic proximity to the restoration site (relaxed local provenance). Defining a “local” provenance is a difficult task and is rarely articulated well in papers that discuss this issue, which hinders progress in the provenancing debate. Adopting a genetically informed definition of a local provenance is probably the most useful approach, and examples include spatial delineation of provenances based on significant genetic differen- tiation in neutral and/or adaptive genetic markers or functional traits. However, such an approach is perhaps the least attainable for practitioners because of the costs, time, and skills required. Local provenancing: Only using a local provenance. Outbreeding depression: The decreased fitness of the hybrid product between two divergent provenances due to disruption of locally adapted gene complexes. Provenance: The geographic location of a seed source that is used to describe the genetic material from that location. Provenancing: In an ecological restoration context, refers to a seed-sourcing strategy, with a focus on the geographic location of seed source(s). Phenotypic plasticity: The nongenetic capability of one genotype to produce a variety of different . Predictive provenancing: Deriving a matched seed source with predicted future home-site conditions; optimally should be based on provenance trials. Restoration: The process of reducing the damage and/or degradation of an by resetting the trajectory of the ecological toward that of a reference state. This definition should potentially be broadened to capture restoration of sites that do not have a reference (e.g., pollinator habitat in agricultural matrices or biodiverse urban green spaces) and to also include sites that have been degraded to such an extent that restoration to a reference state is likely an unachievable goal (e.g., some postmining sites and novel ecosystems). Seed zones: Discrete geographic regions that have similar environments. Transfer within zones should result in few detrimental effects on mean population fitness. Optimally should be based on progeny testing of multiple provenances.

knowledge gaps from science into practice, and ultimately Improving provenance strategy choice. Local provenancing has improve restoration outcomes now and in the future. been the preferred approach for many years. However, a strict interpretation of local provenancing may halt restora- Strategic goals and practitioner priorities tion projects if local seed supply is insufficient (Wilkinson We identify four gaps in provenance decision-making that 2001, Broadhurst et al. 2008). Local provenancing should are commonly faced by both policymakers and practitio- not be so restrictive that it stops projects, even if this means ners. These include (1) the lack of guidance when depart- that nonlocal provenances are introduced. In cases in ing from a strict local provenancing strategy, (2) the need which broader provenances are used or a change in practice for greater evidence-based restoration practices, (3) the is implemented, documentation and ongoing monitor- potential risks associated with using nonlocal provenances, ing will be important in order to evaluate the impacts of focusing on outbreeding depression, and (4) the risks and such changes on restoration success. Indeed, determin- benefits of using in restoration and when they may ing whether plant failure at a restoration site is due to be required. Each of these are discussed below. provenance selection can be inferred through personal https://academic.oup.com/bioscience July 2018 / Vol. 68 No. 7 • BioScience 511 Forum observations, but without experiments and monitoring, such outcomes. Embedding well-designed common garden exper- evidence remains anecdotal. iments into restoration projects is a demonstrated way to Departing from a strict local provenancing strategy relies obtain empirical evidence on the effect of provenance choice on the development of robust seed transfer guidelines, such (figure 1). Despite the clear benefits of such researcher–prac- as seed zones. Seed zones generally refer to regions that have titioner collaborations, differences in training, terminology, similar environments, and transfer within zones should objectives, and reward systems can create a lag in research result in few detrimental effects on mean population fitness uptake and a barrier to collaboration (Guerrero and Wilson (Hufford and Mazer 2003). Such zones are well developed in 2017). For example, most restoration funders demand many forestry sectors because of large commercial interest on-ground actions over research. There need to be better in the final crop, but they are less well developed for resto- cross-sector communication of the benefits of and increased ration. Ideally, seed zones should reflect the likelihood of funding for embedding experiments into restoration proj- adaptive differentiation of the focal species (Kilkenny 2015, ects. Ultimately, these experiments will help inform future Jørgensen et al. 2016, Bucharova et al. 2017b). Geographic restoration and should become a standard part of as many distance, for example, is often used as the basis of seed trans- restoration projects as possible. fer zones (Mortlock 2000). However, geographic distance Monitoring embedded experiments is a key part of build- is a theoretically poor predictor of adaptive differentiation ing the evidence-based feedback loop into restoration prac- unless it correlates with environmental distance (Leimu and tice (figure 1) and should be prioritized higher by funders to Fischer 2008). Indeed, genetic differentiation among popu- improve provenance decision-making. Monitoring can effi- lations can occur over short distances because of microsite ciently be done by aligning and collaborating with research- differences, as well as over broad scales reflecting clinal ers when, for example, student projects or contracted work variation or more major geographic barriers to gene flow can be undertaken to collect, analyze, and interpret data (Richardson et al. 2014). As such, seed zones should reflect from such experiments (e.g., Bailey et al. 2013, Breed et al. this environmental heterogeneity, because this is likely a 2013, 2016a, Gellie et al. 2016, 2018). In fact, it is often the better predictor of adaptive differentiation than geographic case that researchers seek more opportunities to work with distance (Hereford 2009). Seed zones for restoration have practitioners to broaden the impact of their research (Evans been defined in some countries, such as the provisional and Plewa 2016). Nevertheless, it is important that research- seed zones in the United States (Bower et al. 2014) and ers are brought in early into the restoration process, because Herkunftregionen in Germany (Durka et al. 2017). However, well-designed studies (e.g., with controls and randomized there is a need to develop seed-zone boundaries more gen- treatment replicates) are more powerful than post hoc analy- erally to better reflect ecological and/or genetic differences ses (Bucharova et al. 2017a). Furthermore, the maintenance rather than political boundaries. of well-documented databases on the provenances used in Sourcing seed across political boundaries is a prerequisite the experiments (e.g., geographic location, degree of frag- when nonlocal provenances are used, requiring the exchange mentation, or number of sampled mothers in a bulked seed- of seed from outside and potentially across established sup- lot) will assist in interpreting the data generated from such ply networks (i.e., among seed collectors and/or producers). experiments and help to determine the factors influencing Creating a mechanism to share seed across political bound- long-term success in restoration projects. However, there aries will further help to achieve better restoration results are few examples of good provenance-recording frameworks through greater provenance options. Indeed, stakeholders that allow such monitoring and analysis to take place in the in the United States have developed a strategic framework absence of research collaborations. Implementing a track- to help alleviate provenance supply issues, with the goal of ing system, such as the yellow-tag system employed in the improving the availability of appropriate seed for restoration. United States (Young 1996), could improve the quality of To increase the cost-effectiveness and availability of appropri- provenance information across the provenance supply chain. ate seed, the Plant Conservation Alliance (2015) developed the National Seed Strategy for Rehabilitation and Restoration, Mitigate the risk of outbreeding depression. The risks associ- which fosters coordination among parties involved along the ated with mixing provenances for restoration have been seed supply chain, from wild seed co­ llection to the applica- thoroughly discussed (e.g., maladaptation and outbreed- tion in restoration projects. Similar strategic frameworks exist ing depression; see Byrne et al. 2011, Weeks et al. 2011). elsewhere (e.g., in São Paulo state, Brazil; Chaves et al. 2015). Unlike maladaptation, which is difficult to predict, there are We encourage formulation of such frameworks in other practical recommendations about how to predict outbreed- counties, because they will likely help (a) establish best-prac- ing depression—the reduced fitness of progeny resulting tice provenance decision-making, (b) manage and potentially from mating between two genetically dissimilar individuals mitigate the risks of poor decision-making, and (c) ultimately (Templeton 1986, Frankham et al. 2011, Weeks et al. 2011). improve accountability of provenance-choice decisions. The risks of outbreeding depression can largely be predicted by identifying whether there are ploidy or major chromo- Growing the evidence base for restoration. There is an increased somal polymorphisms between provenances with karyotyp- need for evidence-based restoration to achieve optimal ing or flow cytometry (Frankham et al. 2011).

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Figure 1. A schematic representation of the evidence-based feedback loop that embedded provenance trials within restoration plantings can have on improving provenance decision-making.

The frequency and phylogenetic patterns of these with ploidy that can be the basis of rapid screening (e.g., seed intraspecies ploidy polymorphisms are an active area of mass in big sagebrush, Asteraceae; Richardson et al. 2015). Taxa research. The publicly available Chromosome Counts in Asteraceae and Poaceae should be priority candidates for Database (CCDB; Rice A et al. 2015) indicates that ­further ploidy screening when used for restoration, because of approximately 16% of plant species show ploidy polymor- their apparent high frequency of intraspecies . phisms. However, only 69 polymorphic species have been well sampled (i.e., range-wide and n > 100 sampling; Kolář When to use cultivars. Restoration often takes place at sites that et al. 2017). Of these 69 species, 21 were Asteraceae and have deviated far away from their reference state, resulting 7 were Poaceae, supporting taxonomic trends identified in novel environments (e.g., high salinity or nutrient levels by Kramer and colleagues (2018). Interestingly, 16% of 39 postagriculture and novel postmining). It may be dif- species in Kolář and colleagues (2017) showed intrapopu- ficult to establish native seed, regardless of provenance, at lation polymorphisms, indicating that ploidy variation these sites. In such cases, selectively bred cultivars may be between and within populations may occur at similar rates. appropriate. Indeed, the use of cultivars in restoration has Inexpensive checks for ploidy polymorphisms should be gained momentum, particularly in the United States. The more broadly employed, especially for plant groups expected genetic background of cultivars can vary greatly, with some to exhibit intraspecies ploidy differences, to improve long-term being clonal or highly inbred, whereas others are derived restoration success by helping to mitigate the risk of outbreeding from polycrosses consisting of multiple pollen parents from depression. For example, ploidy of species used for restoration the same or different provenances. should be initially screened in publically available databases (e.g., The use of cultivars may be problematic if they lack the CCDB). For some species, there are phenotypic correlates genetic variation or if they have traits that counteract the https://academic.oup.com/bioscience July 2018 / Vol. 68 No. 7 • BioScience 513 Forum restoration process (Chivers et al. 2016, Nevill et al. 2016). they are often based on environmental layers that assume Furthermore, when cultivars have a narrow genetic base, equal weighting of these factors on fitness. Extensions of they risk generating genetically uniform populations that these models to include both genetic information (Kilkenny may be less resilient to responding to environmental changes 2015, Ikeda et al. 2017) and ecophysiological limits (e.g., compared with those produced by wild provenances. The mechanistic models; Kearney et al. 2009, Caddy-Retalic habitat provided by these cultivars can also have a negative et al. 2017) provide an increased realism to their predic- impact on dependent organisms in terms of both supporting tions. However, further research is required, with an initial a limited set of species and disrupting ecosystem functions focus on key species used in restoration. Predictions of plant (Barbour et al. 2016, Mody et al. 2017). Nevertheless, the performance based on habitat suitability models need to be use of polycrosses may counteract some of these concerns empirically validated through reciprocal transplant experi- (Chivers et al. 2016). We emphasize that cultivars should ments or at least an understanding of the role climate and be used in a risk-assessment framework to minimize their nonclimate factors have on the study system. impact on natural populations (Byrne et al. 2011, Weeks et al. 2011). Components of local adaptation. Populations are often locally adapted (Leimu and Fischer 2008, Hereford 2009, Oduor Research priorities et al. 2016). Local adaptation can have both climate and The push for greater evidence-based provenance decision- many nonclimate components, including other abiotic fac- making has highlighted several key areas for future research. tors such as soil and photoperiod (Savolainen et al. 2013, These include (a) understanding the role of phenotypic Christmas et al. 2016a), but biotic factors such as antagonists plasticity in climate resilience of provenances, (b) developing and mutualists are also important (Crémieux et al. 2008, improved species habitat suitability models to guide prov- Gellie et al. 2016, Potts et al. 2016, Gehring et al. 2017, Urbina enance choice, (c) understanding provenance adaptation to et al. 2018). Some nonlocal provenances may have no history both biotic and abiotic factors, and (d) understanding the of exposure to local pests and pathogens (Potts et al. 2016), provenance effects on dependent organisms in restoration and pests and pathogens may themselves be shifting their plantings. Each of these are discussed below. ranges (Burke et al. 2017), potentially increasing the risk of maladaptation (Gellie et al. 2016). Little is known about the Phenotypic plasticity. The capability of one genotype to produce relative importance of climate compared with these other a variety of different phenotypes—phenotypic plasticity—is factors for most plant species, but reciprocal transplant and poorly understood for most species used in restoration. experimental treatments (e.g., and pathogen exclu- Despite this poor understanding, plasticity will likely be sion or exposure trials) can help tease these effects apart. important in a restoration context because it can allow short- term acclimation to novel environments and thereby stabilize Ecological networks. The debate on seed-sourcing strategies fitness during environmental change (Nicotra et al. 2010). has generally focused on mean provenance fitness. However, Phenotypic plasticity can be quantified by growing genotypes there are largely unappreciated extended effects of prov- in a variety of environments (e.g., with and without herbi- enance choice on organisms that colonize and inhabit resto- vores or across an ) and determining ration plantings (Whitham et al. 2006, Crémieux et al. 2008, the variation in traits produced by each genotype across Bucharova 2017). Provenance effects have been shown to environments. A broader understanding of plasticity in func- affect individual organism responses, as well as biotic com- tional and fitness traits (e.g., water-use efficiency, specific leaf munities both above- (Bucharova et al. 2016, Gosney et al. area, and relative growth rate) from theoretical, empirical, 2017) and belowground (Senior et al. 2016, Gehring et al. and applied-research perspectives would help provenance 2017, Urbina et al. 2018). The coevolutionary relationships decision-making by understanding how trait plasticity within between local provenances and their dependent communities a particular provenance influences its potential to survive and (e.g., Toju and Sota 2005, Gehring et al. 2017) further empha- persist under changing conditions (e.g., McLean et al. 2014). size the importance of considering the extended effects of Although there is clear theoretical understanding of the using local or nonlocal provenances on ecological networks. potential benefits of plasticity, such as facilitating rapid evolu- tion (Rice and Emery 2003) that increases climate resilience Conclusions of restoration plantings, there is a greater need to evaluate its The restoration sector aims to return biodiverse, func- importance for provenance decision-making. tional ecosystems at unprecedented scales (Verdone and Seidl 2017), as well as to restore valuable ecosystem ser- Habitat suitability models. A principal concern in the seed- vices (see the Call to Action from the 2017 Society for sourcing debate is climate change, and much of our current Ecological Restoration conference at www.ser.org/general/ predictive knowledge relies on habitat suitability models that custom.asp?page=7thWorldConference). However, the a­bility incorporate climate projections (Elith and Leathwick 2009). to meet these aspirational goals relies on supplying vast Although habitat suitability models provide a way to select quantities of appropriately provenanced seed. Although the provenances for restoration plantings (Harrison et al. 2017), suitability of different provenancing strategies will no doubt

514 BioScience • July 2018 / Vol. 68 No. 7 https://academic.oup.com/bioscience Forum be context dependent, the debate continues. To progress the Bucharova A, Michalski S, Hermann JM, Heveling K, Durka W, Hölzel N, debate from largely theoretical to empirical underpinnings, Kollmann J, Bossdorf O. 2017b. Genetic differentiation and regional adaptation among seed origins used for grassland restoration: Lessons we recommend here a set of priority actions that need to be from a multispecies transplant experiment. Journal of Applied adopted to improve restoration outcomes from provenance 54: 127–136. decision-making: (a) Increase testing of provenance deci- Burke JL, Bohlmann J, Carroll AL. 2017. Consequences of distributional sions by embedding provenance experiments into restoration asymmetry in a warming environment: Invasion of novel forests by the projects. (b) Develop policies and standards on provenance mountain pine beetle. Ecosphere 8 (art. e01778). 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All the authors have an interest in the science and practice of seed sourc- Nicotra AB, et al. 2010. Plant phenotypic plasticity in a changing climate. ing and provenance decision-making for restoration. Martin Breed (martin. Trends in Plant Science 15: 684–692. [email protected]), Nick Gellie, and Andrew Lowe are with the School Oduor AM, Leimu R, Kleunen M. 2016. Invasive plant species are locally of Biological Sciences and the Environment Institute at the University of adapted just as frequently and at least as strongly as native plant species. Adelaide, in Australia. Armin Bischoff is at the University of Avignon, in Journal of Ecology 104: 957–968. France. Paula Durruty is at the Instituto Forestal Nacional (INFONA), in Petit RJ, Sheng Hu F, Dick CW. 2008. Forests of the past: A window to future San Lorenzo, Paraguay. Emily Gonzales is with the Ecological Restoration changes. Science 320: 1450–1452. Division at Parks Canada, in Vancouver, British Columbia. 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Forest Ecology and Management 368: Big Hole Watershed Committee, in Divide, Montana. Paul Nevill is with 183–193. the Department of Environment and Agriculture at Curtin University, in Prober SM, Byrne M, McLean EH, Steane DA, Potts BM, Vaillancourt Australia. Anna Bucharova ([email protected]) RE, Stock WD. 2015. Climate-adjusted provenancing: A strategy is with the Department of Plant at Karl Eberhard for climate-resilient ecological restoration. Frontiers in Ecology and University and with the Department of and Nature Evolution 3 (art, 65). Conservation at Albert Ludwigs University, in Freiburg, Germany.

516 BioScience • July 2018 / Vol. 68 No. 7 https://academic.oup.com/bioscience